Experimental cortical stroke induces aberrant increase of sharp-wave-associated ripples in the hippocampus and disrupts cortico-hippocampal communication

J Cereb Blood Flow Metab. 2020 Sep;40(9):1778-1796. doi: 10.1177/0271678X19877889. Epub 2019 Sep 26.

Abstract

The functional consequences of ischemic stroke in the remote brain regions are not well characterized. The current study sought to determine changes in hippocampal oscillatory activity that may underlie the cognitive impairment observed following distal middle cerebral artery occlusion (dMCAO) without causing hippocampal structural damage. Local field potentials were recorded from the dorsal hippocampus and cortex in urethane-anesthetized rats with multichannel silicon probes during dMCAO and reperfusion, or mild ischemia induced by bilateral common carotid artery occlusion (CCAO). Bilateral change of brain state was evidenced by reduced theta/delta amplitude ratio and shortened high theta duration following acute dMCAO but not CCAO. An aberrant increase in the occurrence of sharp-wave-associated ripples (150-250 Hz), crucial for memory consolidation, was only detected after dMCAO reperfusion, coinciding with an increased occurrence of high-frequency discharges (250-450 Hz). dMCAO also significantly affected the modulation of gamma amplitude in the cortex coupled to hippocampal theta phase, although both hippocampal theta and gamma power were temporarily decreased during dMCAO. Our results suggest that MCAO may disrupt the balance between excitatory and inhibitory circuits in the hippocampus and alter the function of cortico-hippocampal network, providing a novel insight in how cortical stroke affects function in remote brain regions.

Keywords: Local field potential; common carotid artery occlusion; connectivity; distal middle cerebral artery occlusion; modulation index; phase amplitude coupling.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Carotid Stenosis / physiopathology
  • Cerebral Cortex / physiopathology*
  • Cognitive Dysfunction / physiopathology
  • Delta Rhythm
  • Electroencephalography
  • Gamma Rhythm
  • Hippocampus / physiopathology*
  • Infarction, Middle Cerebral Artery / physiopathology
  • Ischemic Stroke / physiopathology*
  • Memory Consolidation
  • Nerve Net / physiopathology*
  • Rats
  • Reperfusion Injury / physiopathology
  • Theta Rhythm